High-level expression of rabbit 15-lipoxygenase induces collapse of the mitochondrial pH gradient in cell culture

Biochemistry

Volumn 43, Issue 48, 2004, Pages 15296-15302

  Vijayvergiya, Chetan ^a,b   De Angelis, Dino ^a   Walther, Matthias ^c   Kühn, Hartmut ^c   Duvoisin, Robert M ^d   Smith, Deborah H ^a   Wiedmann, Martin ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIODEGRADATION; BLOOD; CELL CULTURE; CELLS; PH EFFECTS;

CELLULAR ORGANELLES; MAMMALIAN ERYTHROBLASTS; MITOCHONDRIA; RED BLOOD CELLS;

ENZYME KINETICS;

ARACHIDONATE 15 LIPOXYGENASE; ISOENZYME;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MEMBRANE; CELL ORGANELLE; CELL PH; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MECHANISM; ERYTHROCYTE; ERYTHROPOIESIS; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; RETICULOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ARACHIDONATE 15-LIPOXYGENASE; CELL LINE; CELL MEMBRANE PERMEABILITY; ENZYME ACTIVATION; HUMANS; HYDROGEN-ION CONCENTRATION; INTRACELLULAR MEMBRANES; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; RABBITS; RECOMBINANT PROTEINS; SEQUENCE DELETION; TRANSFECTION;

ANIMALIA; MAMMALIA; ORYCTOLAGUS CUNICULUS;

EID: 10044255242     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048745v     Document Type: Article

References (32)

1. Schewe, T., Rapoport, S. M., and Kuhn, H. (1986) Enzymology and physiology of reticulocyte lipoxygenase: comparison with other lipoxygenases, Adv. Enzymol. Relat. Areas Mol. Biol. 58, 191-272.
2. Klein, R. F., Allard, J., Avnur, Z., Nikolcheva, T., Rotstein, D., Carlos, A. S., Shea, M., Waters, R. V., Belknap, J. K., Peltz, G., and Orwoll, E. S. (2004) Regulation of bone mass in mice by the lipoxygenase gene Alox15, Science 303, 229-232.
3. Shureiqi, I., Jiang, W., Zuo, X., Wu, Y., Stimmel, J. B., Leesnitzer, L. M., Morris, J. S., Fan, H. Z., Fischer, S. M., and Lippman, S. M. (2003) The 15-lipoxygenase-1 product 13-S-hydroxyoctadecadienoic acid down-regulates PPAR-delta to induce apoptosis in colorectal cancer cells, Proc. Natl. Acad. Sci. U.S.A. 100, 9968-9973.
4. Wong, B. C., Wang, W. P., Cho, C. H., Fan, X. M., Lin, M. C., Kung, H. F., and Lam, S. K. (2001) 12-Lipoxygenase inhibition induced apoptosis in human gastric cancer cells, Carcinogenesis 22, 1349-1354.
5. Los, M., Schenk, H., Hexel, K., Baeuerle, P. A., Droge, W., and Schulze-Osthoff, K. (1995) IL-2 gene expression and NF-kappa B activation through CD28 requires reactive oxygen production by 5-lipoxygenase, EMBO J. 14, 3731-3740.
6. Huang, J. T., Welch, J. S., Ricote, M., Binder, C. J., Willson, T. M., Kelly, C., Witztum, J. L., Funk, C. D., Conrad, D., and Glass, C. K. (1999) Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase, Nature 400, 378-382.
7. Samuelsson, B., Haeggstrom, J. Z., and Wetterholm, A. (1991) Leukotriene biosynthesis, Ann. N. Y. Acad. Sci. 629, 89-99.
8. Rapoport, S. M., Schewe, T., Wiesner, R., Halangk, W., Ludwig, P., Janicke-Hohne, M., Tannert, C., Hiebsch, C., and Klatt, D. (1979) The lipoxygenase of reticulocytes. Purification, characterization and biological dynamics of the lipoxygenase; its identity with the respiratory inhibitors of the reticulocyte. Eur. J. Biochem. 96, 545-561.
9. Boyington, J. C., Gaffney, B. J., and Amzel, L. M. (1993) The three-dimensional structure of an arachidonic acid 15-lipoxygenase, Science 260, 1482-1486.
10. Minor, W., Steczko, J., Bolin, J. T., Otwinowski, Z., and Axelrod, B. (1993) Crystallographic determination of the active site iron and its ligands in soybean lipoxygenase L-1, Biochemistry 32, 6320-6323.
11. Gillmor, S. A., Villasenor, A., Fletterick, R., Sigal, E., and Browner, M. F. (1997) The structure of mammalian 15-lipoxygenase reveals similarity to the lipases and the determinants of substrate specificity, Nat. Struct. Biol. 4, 1003-1009.
12. Chen, X. S., Kurre, U., Jenkins, N. A., Copeland, N. G., and Funk, C. D. (1994) cDNA cloning, expression, mutagenesis of C-terminal isoleucine, genomic structure, and chromosomal localizations of murine 12-lipoxygenases, J. Biol. Chem. 269, 13979-13987.
13. Kühn, H., Belkner, J., Wiesner, R., and Brash, A. R. (1990) Oxygenation of biological membranes by the pure reticulocyte lipoxygenase, J. Biol. Chem. 265, 18351-18361.
14. Brinckmann, R., Schnurr, K., Heydeck, D., Rosenbach, T., Kolde, G., and Kühn, H. (1998) Membrane translocation of 15-lipoxygenase in hematopoietic cells is calcium-dependent and activates the oxygenase activity of the enzyme. Blood 91, 64-74.
15. van Leyen, K., Duvoisin, R. M., Engelhardt, H., and Wiedmann, M. (1998) A function for lipoxygenase in programmed organelle degradation, Nature 395, 392-395.
16. Yokota, S., Oda, T., and Fahimi, H. D. (2001) The role of 15-lipoxygenase in disruption of the peroxisomal membrane and in programmed degradation of peroxisomes in normal rat liver, J. Histochem. Cytochem. 49, 613-622.
17. Maccarrone, M., Melino, G., and Finazzi-Agro, A. (2001) Lipoxygenases and their involvement in programmed cell death, Cell Death Differ. 8, 776-784.
18. Walther, M., Wiesner, R., and Kühn, H. (2004) Investigations into calcium-dependent membrane association of 15-lipoxygenase-1. Mechanistic roles of surface-exposed hydrophobic amino acids and calcium, J. Biol. Chem. 279, 3717-3725.
19. Gasko, O., and Danon, D. (1972) Deterioration and disappearance of mitochondria during reticulocyte maturation, Exp. Cell Res. 75, 159-169.
20. Geminard, C., de Gassart, A., and Vidal, M. (2002) Reticulocyte maturation: mitoptosis and exosome release. Biocell 26, 205-215.
21. Bassnett, S., and Beebe, D. C. (1992) Coincident loss of mitochondria and nuclei during lens fiber cell differentiation, Dev. Dyn. 194, 85-93.
22. Bassnett, S. (1992) Mitochondrial dynamics in differentiating fiber cells of the mammalian lens, Curr. Eye Res. 11, 1227-1232.
23. Grullich, C., Duvoisin, R. M., Wiedmann, M., and van Leyen, K. (2001) Inhibition of 15-lipoxygenase leads to delayed organelle degradation in the reticulocyte, FEBS Lett. 489, 51-54.
24. Kühn, H., Schewe, T., and Rapoport, S. M. (1984) The inactivation of lipoxygenases by acetylenic fatty acids, Biomed. Biochim. Acta 43, S358-S361.
25. Llopis, J., McCaffery, J. M., Miyawaki, A., Farquhar, M. G., and Tsien, R. Y. (1998) Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins, Proc. Natl. Acad. Sci. U.S.A. 95, 6803-6808.
26. Schaffner, W., and Weissmann, C. (1973) A rapid, sensitive, and specific method for the determination of protein in dilute solution, Anal. Biochem. 56, 502-514.
27. Walter, P., and Blobel, G. (1983) Preparation of microsomal membranes for cotranslational protein translocation, Methods Enzymol. 96, 84-93.
28. Miesenbock, G., De Angelis, D. A., and Rothman, J. E. (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins, Nature 394, 192-195.
29. Ostareck, D. H., Ostareck-Lederer, A., Shatsky, I. N., and Hentze, M. W. (2001) Lipoxygenase mRNA silencing in erythroid differentiation: The 3′UTR regulatory complex controls 60S ribosomal subunit joining, Cell 104, 281-290.
30. Hurt, E. C., Pesold-Hurt, B., Suda, K., Oppliger, W., and Schatz, G. (1985) The first twelve amino acids (less than half of the pre-sequence) of an imported mitochondrial protein can direct mouse cytosolic dihydrofolate reductase into the yeast mitochondrial matrix, EMBO J. 4, 2061-2068.
31. Rouslin, W., and Broge, C. W. (1989) Regulation of mitochondrial matrix pH and adenosine 5′-triphosphatase activity during ischemia in slow heart-rate hearts. Role of Pi/H+ symport, J. Biol. Chem. 264, 15224-15229.
32. Chacon, E., Reece, J. M., Nieminen, A. L., Zahrebelski, G., Herman, B., and Lemasters, J. J. (1994) Distribution of electrical potential, pH, free Ca2+, and volume inside cultured adult rabbit cardiac myocytes during chemical hypoxia: a multiparameter digitized confocal microscopic study, Biophys. J. 66, 942-952.